Oceanic forcing of coral reefs.

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Review in Advance first posted online on September 17, 2014. (Changes may still occur before final publication online and in print.)

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Annu. Rev. Marine. Sci. 2015.7. Downloaded from www.annualreviews.org by WIB6105 - Technische Universitaet Muenchen Universitaetsbibliothek (aka University Technische Munchen) on 11/11/14. For personal use only.

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Oceanic Forcing of Coral Reefs Ryan J. Lowe and James L. Falter ARC Centre of Excellence for Coral Reef Studies, School of Earth and Environment, and UWA Oceans Institute, University of Western Australia, Crawley 6009, Australia; email: [email protected], [email protected]

Annu. Rev. Mar. Sci. 2015. 7:18.1–18.24

Keywords

The Annual Review of Marine Science is online at marine.annualreviews.org

coral reefs, waves, tides, circulation, temperature, nutrients

This article’s doi: 10.1146/annurev-marine-010814-015834

Abstract

c 2015 by Annual Reviews. Copyright All rights reserved

Although the oceans play a fundamental role in shaping the distribution and function of coral reefs worldwide, a modern understanding of the complex interactions between ocean and reef processes is still only emerging. These dynamics are especially challenging owing to both the broad range of spatial scales (less than a meter to hundreds of kilometers) and the complex physical and biological feedbacks involved. Here, we review recent advances in our understanding of these processes, ranging from the small-scale mechanics of flow around coral communities and their influence on nutrient exchange to larger, reef-scale patterns of wave- and tide-driven circulation and their effects on reef water quality and perceived rates of metabolism. We also examine regional-scale drivers of reefs such as coastal upwelling, internal waves, and extreme disturbances such as cyclones. Our goal is to show how a wide range of ocean-driven processes ultimately shape the growth and metabolism of coral reefs.

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1. INTRODUCTION Upwelling: the upward movement of water resulting from wind-driven Ekman transport or flow curvature in the vicinity of islands Internal waves: wave motions that propagate within the interior of a density-stratified ocean

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The physics, chemistry, and biology of the world’s oceans have long been known to play a critical role in shaping the growth, diversity, and distribution of coral reefs. Darwin (1842) first hypothesized that the surrounding oceans provide a major source of nutrition to coral reef communities and that reefs therefore grow best at their most seaward edges. More than a century later, Munk & Sargent (1954) proposed that the energy dissipated by waves on shallow fore reefs and reef crests facilitates the rapid exchange of nutrients and other metabolites necessary to support the robust growth of reef communities in otherwise nutrient-poor environments. This basic idea would stimulate modern research aimed at understanding how hydrodynamic processes in benthic boundary layers control the uptake of dissolved nutrients by reef communities (Atkinson & Bilger 1992, Falter et al. 2004, Hearn et al. 2001, Lowe et al. 2005b, Thomas & Atkinson 1997). Additional work has since provided more direct evidence of how reefs also feed off the living plankton washed over them from the surrounding ocean (Ayukai 1995, Charpy & Blanchot 1999, Fabricius et al. 1998, Wyatt et al. 2010). Nevertheless, the same ocean waves driving the circulation and material exchange that are beneficial to the growth of reef organisms can also act as a destructive force when large enough, especially when they are generated by large storms such as tropical cyclones (Massel & Done 1993, Woodley et al. 1981). Extreme wave events can act as an additional source of physical stress on reef systems already contending with other forms of environmental disturbance (De’ath et al. 2012) and may also lead to long-term changes in reef community structure and diversity (Dollar & Tribble 1993, Madin & Connolly 2006). The environment in which reefs live is further shaped by ever-changing ocean conditions at scales much greater than the reef itself. At the shelf or island scale, coastal upwelling caused by wind-driven Ekman transport or generated in the lee of islands can bring up cooler, more nutrientand particle-rich water. Such environments can support higher rates of nutrient acquisition (Gove et al. 2006, Wyatt et al. 2010), create adverse chemical conditions for the formation of biogenic carbonate minerals (Manzello 2010), and offer potential refugia against ocean warming (Karnauskas & Cohen 2012). Nonlinear internal waves propagating up continental shelf and island slopes provide another potential mechanism for transporting cool water and nutrients to shallow coral reefs (Leichter et al. 1996, Wang et al. 2007). At even larger scales, regional circulation patterns control the widespread dispersal of reef larvae and, therefore, the biogeographical distribution of reef organisms (e.g., Richmond 1987, Shulman & Bermingham 1995). In the future, the oceans will continue to play an important role in determining how global climate trends such as increased warming and the dissolution of CO2 will manifest themselves, or “downscale,” at the regional, coastal, shelf, reef, community, and ultimately organism scales. For example, although mean global temperatures are expected to increase by ∼4◦ C by the end of the century under a business-as-usual scenario (Meinshausen et al. 2009), seasonal warming events driving sea surface temperature anomalies of several degrees are already a regular occurrence. Such intense ocean warming events occurred across the western Pacific and Caribbean in 1998 owing to particularly intense El Nino ˜ conditions (e.g., Bruno et al. 2001, McClanahan et al. 2004) and along Western Australia in 2010–2011 owing to the intensification of a warm eastern boundary current during an intense La Nina ˜ period (Depczynski et al. 2013, Moore et al. 2012). Within the reef systems themselves, benthic production, respiration, and net calcification can alter the chemistry of circulating water (Kinsey 1978, Odum & Odum 1955, Sargent & Austin 1949, Smith 1973); however, the magnitudes of these changes depend just as much on the degree of hydrodynamic forcing and the morphologies of the reef systems as they do on rates of benthic metabolism (Falter et al. 2013, Venti et al. 2012, Zhang et al. 2012). Thus, changes in the global wave and storm climate that are expected to occur over the next century (Young et al. 2011) will no doubt

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lead to concomitant changes to many of the above biogeochemical and ecological processes on reefs. It is clear that the growth, metabolism, and community structure of coral reefs are heavily influenced by the oceanic environment in which they live. Unfortunately, it is not possible for a single review to cover all important aspects of the coupling between physical and biological processes on coral reefs. There have been some prior efforts to summarize the influence of oceanic processes on coral reefs, although these either were published several decades ago (Hamner & Wolanski 1988) or focused mainly on the details of the prevalent hydrodynamic processes (Monismith 2007). To provide what we think is a good balance between breadth and detail, the present review focuses first on the small- and reef-scale hydrodynamic processes affecting the transport and transfer of mass (nutrients and carbon, dissolved and particulate), heat (temperature), and momentum (drag and dissipation) on reefs, and second on how offshore ocean processes affect the physical and chemical properties of nearshore reef waters. The review is thus organized by scale, starting with the smallest scales (individual reef organisms and canopies; Section 2), moving to intermediate scales (reef communities and systems; Section 3), and concluding with the largest scales that influence the growth and development of reefs along the continental margins and oceanic island groups (regional and global; Section 4). For reference, Table 1 summarizes the variables used throughout the review.

Canopy flow: a region of flow inside the bottom roughness layer created by reef organisms

2. ORGANISM TO REEF CANOPY SCALES (0.1–10 m) The flow structure in and around reef organisms depends on the complex interactions between the overlying water motion and the typically large, three-dimensional bottom roughness (or canopies) formed by reef organisms (Figure 1a,b). The flow dynamics throughout reef canopies are highly analogous to other, more well-studied canopy flows, particularly those through seagrasses and other aquatic vegetation (for a recent review, see Nepf 2012). The common challenge for understanding the flow dynamics in all natural canopies is properly accounting for the highly variable spatial flow structure that arises within even the simplest morphologies. There have been some attempts to directly observe or numerically simulate the full three-dimensional turbulent flow structure through individual branching coral colonies (Chang et al. 2009, Chindapol et al. 2013, Kaandorp et al. 2003); however, such efforts are extremely expensive computationally, requiring flows to be resolved down to scales on the order of millimeters. Thus, it remains impractical to resolve the roughness geometries of reef organisms at the scale of entire reef communities or systems. To account for how such unresolved small-scale hydrodynamic processes influence the largerscale macroscopic properties of a canopy flow (e.g., mean velocity profiles), the traditional Reynolds-averaged Navier-Stokes momentum equations are spatially averaged over a horizontal plane that excludes the solid canopy elements (Raupach & Shaw 1982): 1 ∂P 1 ∂τxy Du =− + − fx , Dt ρ ∂x ρ ∂z

(1)

where x is the streamwise direction, z is the vertical direction, ρ is the seawater density, u is the streamwise velocity, P is the pressure, τxy is the shear stress, and the brackets indicate spatially averaged variables. Importantly, the term fx represents a spatially averaged canopy resistance term that arises from forces exerted by the canopy onto the surrounding flow (Lowe et al. 2005a). Ultimately, the fundamental challenge in predicting flow through coral reef canopies via Equation 1 remains how to most accurately relate fx to the complicated three-dimensional structure of reef communities, especially given their abundant variation in morphologies and roughness scales. www.annualreviews.org • Oceanic Forcing of Coral Reefs


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Table 1 Summary of variables used in this review


Variable

Unit

Description

A∞

m

Wave orbital excursion amplitude

C

—

Water column species concentration

Cd,c

—

Canopy element drag coefficient

CD

—

Total bed-form drag coefficient

CM

—

Canopy element inertial force coefficient

fx

m s−1

Spatially averaged canopy resistance

h

m

Water depth

hc

m

Canopy height

hr

m

Depth of the reef flat

H0

m

Offshore wave height

Hs

m

Significant wave height

J

mol m−2 h−1 W m−2

Net flux of heat or mass across the benthic and/or air-sea interface

K

m2 s−1

Horizontal dispersion coefficient

Lr

m

Length of the reef flat from crest to backreef

MTR

m

Mean tidal range

P

kg m−1 s−2

Pressure

q

m2 s−1

Depth-integrated transport

q

m2 s−1

Two-dimensional depth-integrated transport vector

Rek

—

Roughness Reynolds number

S

m d−1

First-order nutrient uptake rate coefficient

Sc

—

Schmidt number

T

◦C

Temperature

TA

μeq kg−1

Total alkalinity

u U¯

m

s−1

m s−1

Depth-averaged current velocity

U∞ Uˆ

m s−1

Free stream velocity

m s−1

Canopy depth-averaged streamwise velocity

α

—

Canopy flow attenuation parameter

β

m−1

Porous media drag parameter

η

m

Dynamic sea level or wave setup

λf

—

Frontal area canopy geometry parameter

τcan

kg m−1 s−2

Shear stress at the top of the canopy

τw

s

Wave period

τRT

h

Residence time of water within the reef domain

Horizontal spatially averaged streamwise velocity

For natural canopies with simple morphologies (e.g., seagrasses), these form-drag forces can be readily parameterized using a quadratic drag law that depends on the local in-canopy velocity, the integrated frontal area of the canopy elements per unit area of the seafloor (λf ), and an empirical drag coefficient (Cd,c ) (for details, see Nepf 2012). Such approaches have been applied to coral reef canopies with well-defined branch geometries (e.g., Figure 1a) (Lowe et al. 2005a); however, the complex morphologies of most reef canopies (e.g., Figure 1b) make assigning a representative λf difficult or even impossible because of the challenge of identifying singular, well-defined geometric parameters. As an alternative approach to address this issue, Lowe et al. (2008) used turbulent 18.4

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a

b

Currents

c

Waves

‹u›(z)

τcan

d

‹u›

(z)

rms

τcan dP/dx

Figure 1 (a,b) Examples of bottom roughness on reefs, showing a homogeneous community of Porites compressa forming a canopy of regular cylindrical branches (panel a; photograph by R.J. Lowe) and a more complex reef canopy of plating and branching Acropora spp. (panel b; photograph by S. Long, Western Australia Department of Parks and Wildlife). (c,d ) Flow structure under different conditions. Under unidirectional flow (panel c), the shear stress at the top of the canopy (τcan ) transfers momentum from the overlying flow field into the canopy and is opposed by the canopy drag forces that attenuate the flow (u) inside the canopy. Under wave-driven oscillatory flow (panel d ), the unsteady wave-induced pressure gradient (∂ P/∂ x) provides an additional source of momentum that substantially increases the rms flow (urms ) inside the canopy for a given flow speed.

porous media flow theory to parameterize fx . The advantage of the porous media approach is that it has already been applied to a number of complex geometrical arrays and tested with a wealth of empirical data (Macdonald et al. 1979). Although this approach has worked well for predicting flow through a community of Porites compressa coral (Lowe et al. 2008), further work is needed to parameterize flow resistance across a broader spectrum of natural reef canopy types.

2.1. Unidirectional Flow For a unidirectional current over a submerged reef canopy, the discontinuity in form drag fx near the top of the canopy generates a region of strong shear in the mean velocity profile (Equation 1), www.annualreviews.org • Oceanic Forcing of Coral Reefs


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Unconfined flow: the flow that occurs when the water depth is much greater than the canopy height; the canopy flow is driven by a shear layer Depth-limited flow: the flow that occurs when the water depth is comparable to the canopy height; the canopy flow is enhanced by the pressure gradient Emergent flow: the flow that occurs when the canopy reaches the water surface; the canopy flow is driven solely by the pressure gradient

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resulting in a local peak in the turbulent shear stress τcan (Ghisalberti 2009) (Figure 1c). The shear layer transfers momentum from the overlying water column down into the canopy, thus driving flow inside the canopy. This is the dominant form of momentum transfer that occurs when the flow is unconfined, or when the canopy height hc occupies only a small fraction of the total water depth h. When hc becomes an appreciable fraction of the water depth, the underlying canopy flow becomes depth limited, and the background pressure gradient driving the overlying flow also starts to directly drive flow within the canopy itself (Nepf & Vivoni 2000). As h c / h increases, the pressure gradient term continues to increase the in-canopy flow, reaching a limit where the reef canopy becomes emergent (h c ∼ h) such that the shear layer is no longer present and flow is driven entirely through the canopy by the external pressure gradient (Nepf 2012). At typical reef canopy heights (ranging from tens of centimeters to meters), many or most flows on coral reef flats (h typically 1–2 m) must experience some degree of depth limitation. This seemingly local effect can also have important consequences for the broader circulation patterns on reefs (hundreds to thousands of meters), as the larger drag forces that arise from more water being driven through a canopy under depth-limited conditions increases the resistance experienced by the overlying flow. This was well illustrated by McDonald et al. (2006), who found that the community bottom-drag coefficient CD, which relates the total drag force to the overlying flow speed (not to be confused with the canopy element drag coefficient Cd,c , described above), increased by roughly two orders of magnitude (from ∼0.01 to 1) as the depth over a canopy of P. compressa coral approached the emergent limit (see figure 3 in McDonald et al. 2006). Furthermore, there appears to be a relatively abrupt transition to high (order 0.1–1) values of CD when h c / h increases above ∼0.3 (Lowe et al. 2008, McDonald et al. 2006). Collectively, these studies emphasize that careful consideration of the in-canopy momentum dynamics—a factor that has been largely ignored in traditional coastal ocean models—is critical to accurately parameterize the effects of bottom drag on reefs (Rosman & Hench 2011).

2.2. Wave-Driven Flow The dynamics of wave-driven flows through canopies have historically received limited attention, owing largely to the lack of analogous terrestrial canopy models on which to build. Although the momentum equations describing water motion in canopies under oscillatory and unidirectional flows are fundamentally similar, there are two key differences: (a) Surface waves can generate large oscillatory pressure gradients at the dominant wave period T (Figure 1d ), and (b) flow accelerations inside the canopy can add an inertial force that increases the overall flow resistance fx in Equation 1. To account for these effects, Lowe et al. (2005a, 2008) developed a simple model describing the momentum dynamics within submerged canopies under wave-driven oscillatory flow by depth integrating Equation 1 over the canopy region: dUˆ dt

acceleration

=

−

1 dP ρ dx

pressure gradient

+

Cf CM (1 − φ) dUˆ |U ∞ |U ∞ − β|Uˆ |Uˆ − . 2h c φ dt form drag shear stress

(2)

inertial force

Here, Uˆ denotes the spatially averaged in-canopy velocity, Cf is a friction coefficient that relates the magnitude of the shear stress at the canopy interface to the free stream velocity U ∞ , β is a dimensional drag parameter based on a porous media formulation that depends on the internal bed geometry, and CM is an inertial force coefficient (for details, see Lowe et al. 2008). Equation 2 predicts that the acceleration of the in-canopy flow (term 1) depends on the pressure gradient and shear stress terms responsible for driving the flow (terms 2 and 3) and the form drag and inertial forces that oppose it (terms 4 and 5). Lowe et al. (2005a) further defined a flow attenuation 18.6

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rms parameter α ≡ Uˆ rms /U ∞ to be the ratio of the rms wave velocity inside the canopy (Uˆ rms ) to rms ). Above the canopy, where the wave-driven flow is assumed to be that in the free stream (U ∞ inviscid (i.e., above the wave boundary layer), the wave-driven pressure gradient is related solely to the acceleration of the free stream oscillatory flow. Simple scaling arguments show that the importance of this pressure gradient term to the shear stress term increases with the ratio of the wave excursion orbital amplitude (Arms ∞ ) to the roughness height of the canopy (Lowe et al. 2005a):

U rms T Arms shear stress ∼ ∞ ∼ ∞ . pressure hc hc

(3)

Thus, similar to the case of severely depth-limited unidirectional flow, the pressure gradient imposed by waves substantially enhances flow inside a reef canopy over a pure unidirectional flow of the same magnitude (Figure 1d ). This theory has been supported by experimental studies using both idealized reef canopies and experimental assemblages of real branching coral reef canopies (Lowe et al. 2005a, 2008; Reidenbach et al. 2007), which have all shown that unsteady wave motion substantially enhances the in-canopy flow (by a factor of 5–10 in these particular studies).

Mass-transfer limited: describes conditions under which the rate of uptake or release of a compound is limited by convective transport across a concentration boundary layer

2.3. Nutrient Uptake Pioneering work by Atkinson and others demonstrated that the biological demand for nutrients on reefs is generally so high that rates of nutrient uptake by reef communities are limited by their convective transfer across turbulent boundary layers formed on the surfaces of benthic reef autotrophs (Atkinson & Bilger 1992, Baird & Atkinson 1997, Thomas & Atkinson 1997). Bilger & Atkinson (1992) described these conditions as being “mass-transfer limited,” and adapted a theory originally developed to describe heat and mass transfer to rough surfaces (from the engineering literature) to instead describe nutrient uptake by coral reef communities. Under conditions of mass-transfer limitation, the maximum mass-transfer-limited nutrient uptake rate (Jmax , in mmol m−2 d−1 ) is first order with respect to the concentration of nutrients in the water column (C, in mmol m−3 ), i.e., Jmax = Smax C, where Smax (in m d−1 ) is the first-order nutrient uptake rate coefficient. On coral reefs, the conditions of mass-transfer limitation tend to break down only when dissolved nutrient concentrations are more than two orders of magnitude greater than those naturally occurring in tropical reef waters (Atkinson & Falter 2003). The application of these mass-transfer formulations to the problem of nutrient uptake kinetics in reef communities was an important step because (a) it approached the problem at the more hydrodynamically relevant spatial scale of entire reef communities acting as canopies (see above), rather than just that of individual organisms, and (b) it provided for the first time some predictive capability for how water motion controls nutrient uptake by reef communities. Subsequent experimental work demonstrated the utility of these mass-transfer relationships to predict rates of nutrient uptake for natural reef communities in laboratory flumes simulating pure unidirectional flow (Baird & Atkinson 1997, Thomas & Atkinson 1997). Falter et al. (2004) later simplified Bilger & Atkinson’s (1992) original nutrient uptake formulations, which also incorporated additional experimental data sets: √ CD U ∞ (4) Smax = 0.2 0.58 , Re k Sc where U ∞ is the free stream flow speed, Sc is the Schmidt number of the dissolved nutrient, Re k is the roughness Reynolds number of the flow, and is an empirical constant equal to ∼4 × 104 . It is important to emphasize that CD in Equation 4 is a bulk drag coefficient that relates the total flow resistance exerted by a reef community to the free stream flow speed U ∞ (see above). Owing www.annualreviews.org • Oceanic Forcing of Coral Reefs


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to the practical size limitations of the experimental flumes that were used to develop Equation 4, most of the experimental reef communities reported in the literature occupied up to 50% of the water depth. Thus, these nutrient relationships have been developed almost exclusively under conditions of substantial depth limitation. This explains the high CD values of ∼0.1–0.2 reported in those studies (see summary in McDonald et al. 2006), suggesting that flow, and perhaps nutrient uptake, would be enhanced within the interior regions of those experimental communities. There are still substantial gaps in our understanding of dissolved nutrient uptake by reef communities under oscillatory flow conditions. However, a growing number of reports—including several direct flume observations (Lowe et al. 2005b, Reidenbach et al. 2006, Thomas & Cornelisen 2003, Weitzman et al. 2013) and inferences based on field studies (Bilger & Atkinson 1992, Falter et al. 2004)—have shown that wave-driven oscillatory flows substantially enhance mass-transfer rates, increasing them by factors of 3 or more. Lowe et al. (2005b) asserted that the relevant velocity scale to describe mass transfer should be the in-canopy flow velocity Uˆ rather than the free stream U ∞ because this is the velocity that more directly interacts with the surfaces of organisms within the interior of the canopy. Thus, the enhancement of nutrient uptake under oscillatory flow can be explained by the higher flow speeds induced within coral reef canopies under these conditions. A similar argument can be made for the enhancement of nutrient uptake under depth-limited flow. Nevertheless, many further data are needed, especially for live natural coral reef communities, to develop better nutrient uptake relationships that can be universally applied across a broad range of flow regimes.


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2.4. Particle Uptake The uptake of organic particles by reef heterotrophs can constitute a source of allochthonous nutrients to coral reefs that is as important as the uptake of dissolved nutrients by reef primary producers (Houlbrèque & Ferrier-Pagès 2009), especially for corals recovering from a recent bleaching event (Ferrier-Pagès et al. 2003, Houlbrèque & Ferrier-Pagès 2009, Houlbrèque et al. 2004, Hughes & Grottoli 2013). There is now abundant evidence of living phytoplankton being actively grazed by whole communities of reef organisms as water flows over reefs (Genin et al. 2009; Monismith et al. 2010; Wyatt et al. 2010, 2012; Yahel et al. 1998); however, the phytoplankton biomass within the oligotrophic tropical waters of most coral reefs is generally dominated by the smallest size fraction (i.e., picoplankton 3 m) and local tidal water level gradients can exceed those induced by wave setup fields. In addition, tides can play a more direct role in driving circulation in larger and more enclosed lagoons where the channels connecting the lagoon with the open ocean are relatively narrow. The constricted exchange of water between these lagoons and the open ocean can cause significant phase lags between a lagoon and offshore water levels (e.g., Dumas et al. 2012). Historically, most reef studies have found that wind stresses often play only a minor role in driving the circulation of shallow reefs; however, wind forcing can be important or even dominant in the circulation of deeper and more isolated lagoons (Atkinson et al. 1981, Delesalle & Sournia 1992, Douillet et al. 2001, Lowe et al. 2009a). Unfortunately, the extent to which buoyancy forcing helps drive reef circulation through either temperature- or salinity-driven stratification has received only limited 18.10

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study; however, this forcing may also be important in certain reef systems (Hoeke et al. 2013, Monismith et al. 2006).

3.2. Biogeochemical Transformation of Reef Waters The degree to which any local process occurring within a reef (physical, chemical, or biological) can affect the spatial and temporal variation in water quality is dependent as much on the strength and pattern of circulation as on the process itself. These relationships can be understood either from an Eulerian perspective, in which circulation and changing water quality are considered within a fixed reference frame, or from a Lagrangian perspective, in which changes in water quality are observed within a defined water parcel flowing through a reef system. From an Eulerian perspective, these relationships are best illustrated by the depth-integrated nonconservative transport equation, which shows the mutual dependence of spatial (∂/∂ x,∂/∂ y) and temporal (∂/∂t) changes in water quality on both the transport q and the net flux of heat or mass into the water column J (Falter et al. 2008):

J = h

flux

∂C + q · ∇C − K ∇ 2 C , dispersion ∂t advection

Eulerian: examining a dynamic flow field from the perspective of a fixed frame of reference Lagrangian: examining a dynamic flow field from the perspective of a water parcel moving with the flow

(6)

local

where C is some nonconservative water quality parameter of interest (nutrient concentration, alkalinity, temperature, etc.) and K is a horizontal dispersion coefficient. J can represent the sum of all biogeochemical processes responsible for the uptake or release of nutrients, particles, dissolved inorganic carbon, alkalinity, etc. It can also represent the net exchange of heat, moisture, and gasses across the air-sea interface. Limited field measurements have shown that mass transport resulting from advection is much greater than that resulting from horizontal dispersion (i.e., q·∇C K ∇ 2 C) on shallow, wave-driven reefs (Falter et al. 2008); however, horizontal dispersion could be more important in reefs with strongly sheared two-dimensional circulation patterns. Furthermore, a fully three-dimensional nonconservative transport equation may be necessary to budget the uptake, release, and transport of mass in deeper and more stratified sections of a reef (Genin et al. 2009, Monismith et al. 2010, Teneva et al. 2013). The application of the nonconservative transport equation to model changes in water quality has proven robust for inversely calculating benthic fluxes in shallow reef environments for more than half a century (e.g., Odum & Odum 1955, Smith 1973), albeit through the use of simplified versions of Equation 6. Earlier methodologies discriminated between flow respirometry, which measures changes in water chemistry along one axis (generally oriented in the cross-reef direction) and assumes that J ≈ q x ∂C/∂ x (Barnes & Devereux 1984, Gattuso et al. 1993, Kraines et al. 1997), and the slack-water method, which considers only the time-dependent changes in water chemistry at a specific site and assumes that J ≈ h∂C/∂t (Kinsey 1978, McMahon et al. 2013, Shaw et al. 2012). Both approaches constitute selective simplifications of the same Eulerian nonconservative transport equation shown in Equation 6. The simplification of upstream-downstream applications of flow respirometry tends to be most robust on shallow reef flats where the flow is both reasonably steady and strong (>5 cm s−1 ) and chemical gradients vary only weakly in time such that q x ∂C/∂ x h∂C/∂t. The slack-water simplification generally requires flow speeds to be on the order of ∼1 cm s−1 or less so that the time-dependent term dominates over the advective terms (i.e., h∂C/∂t q ·∇C). This latter condition is particularly difficult to meet for two reasons. First, it requires that the predominant current is very weak yet still strong enough to provide the necessary turbulent stirring to vertically mix the water column, a criterion that can easily be violated (Kinsey 1978). Second, it requires that the horizontal gradients in water quality also be relatively small, a criterion that is difficult to meet for many reefs given that the spatial distributions of www.annualreviews.org • Oceanic Forcing of Coral Reefs


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Water age: the age of a water parcel relative to when it entered a domain (the complement of residence time)

biomass and metabolism are known to vary by an order of magnitude or more (Andréfouët et al. 2001, Atkinson & Falter 2003, Kinsey 1985, Tanaka et al. 2011). One additional process contributing to transport in reef systems is Stokes drift, or the excess mass transport induced by the nonlinearity of waves (Longuet-Higgins & Stewart 1962). Stokes drift is a depth-dependent, Lagrangian property of wave motion and thus cannot be directly measured by time-averaging fixed-point current meter data; however, it can be estimated from local wave measurements at a specific reef site. Stokes drift within the coastal zone can range from several centimeters per second to tens of centimeters per second depending on the water depth, wave height, and wave period (Monismith & Fong 2004). This can cause the total transport to be far greater than that measured by fixed current meters alone, thus potentially distorting perceived rates of material exchange (Falter et al. 2008). Which terms within the general transport equation above (Equation 6) can or cannot be ignored, and whether Stokes drift should be considered, must be carefully assessed for each reef environment on a case-by-case basis. From a Lagrangian perspective, changes in water quality can also be understood by examining the age and history of a water parcel after it enters a reef system (Figure 3a). Spatial circulation patterns control the spatial distribution of local water ages or residence times across reefs and, therefore, the time under which the water’s chemistry can be altered (Andréfouët et al. 2001, Jouon et al. 2006, Lowe et al. 2009a, Zhang et al. 2012). The average water age can range from as short as a few hours in shallower and more seaward reef habitats to days or weeks in deeper and more interior sections of reef systems (Lowe et al. 2009a, Venti et al. 2012, Zhang et al. 2012). The residence times within very deep (>20 m) atoll lagoons can reach several months depending on the size of the atoll and how closed it is with respect to exchange with the ocean (Atkinson et al. 1981, Callaghan et al. 2006, Delesalle & Sournia 1992, Tartinville et al. 1997). Most importantly,

Residence time (h) 40

τRT

a

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ΔT

b

Change in temperature (ºC) 0.8

35

0.7

30

0.6

25

0.5

20

0.4

15

0.3

10

0.2

5

0.1

0

0

ΔTA

c

Change in total alkalinity (μeq kg–1) 100

80

60

40

20

0

Figure 3 Simulations of (a) residence time (τRT ) as well as changes in (b) daily average water column temperature (T ) and (c) daily average water column total alkalinity (TA), both relative to offshore values across Coral Bay, Ningaloo Reef, under typical summer conditions (Zhang et al. 2012, 2013). All simulations shown were performed using the Regional Ocean Modeling System (ROMS) coupled with the spectral wave model Simulating Waves Nearshore (SWAN). The black lines highlight the 4-m isobath. For additional details, see Zhang et al. (2012). Note that the high degree of similarity between T and TA in this application is largely the result of unusually high coral cover within the Coral Bay lagoon—a feature not common in other sections of Ningaloo Reef or in many other Indo-Pacific reef systems. 18.12

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residence times at any reef site can never be considered a static quantity because they are driven by ever-changing wind, wave, and tide conditions. Changes to the properties of a flowing water mass depend not only on the simple age of a water parcel but also on the specific trajectory or streamline that determines the various reef habitats the parcel is exposed to. Without explicit knowledge of the flow path that a given water mass took prior to the measurement of its changed chemistry relative to some reference point (typically offshore waters), it is not possible to know which sections or areas of reef habitat to assign these observed changes to. This is particularly problematic when attempting to calculate benthic fluxes and reaction rates for entire reef systems using bulk estimates of water residence time and local measurements of water chemistry made at specific reef sites (Falter et al. 2013, Venti et al. 2012, Zhang et al. 2012). Nonetheless, changes in the chemistry of offshore waters are generally most rapid over the most seaward several hundred meters of shallow reef flat. These changes can be well described by a simple analytical equation that depends on offshore wave forcing, reef morphology, and the net benthic and surface mass fluxes (Falter et al. 2013): 2 3/4 J Lr , (7) C ∝ √ H 0 τw h r

Albedo: the fraction of solar radiation that a surface or object reflects

where Lr and hr are the length and depth of the reef flat, respectively, and advection is assumed to be the dominant transport term (q · ∇C ∂C/∂t).

3.3. Temperature Variations in Reef Waters The dynamics driving spatial and temporal changes in water temperature across reefs (Figure 3b) are analogous to those driving changes in water chemistry (Figure 3c) because they are both governed by the same fundamental nonconservative transport equation (Equation 6) (Davis et al. 2011, Falter et al. 2014, McCabe et al. 2010, Zhang et al. 2013). The additional heat gained by reef waters from atmospheric exchange can have profound effects on local temperature anomalies and cumulative thermal stresses on reefs (Davis et al. 2011, Falter et al. 2014, McCabe et al. 2010, Pineda et al. 2013, Zhang et al. 2013). In contrast to rates of benthic reef metabolism, which can vary by more than an order of magnitude (Andersson & Gledhill 2013, Kinsey 1985), net heat fluxes are far less spatially variable across reefs. First, spatial variations in atmospheric conditions (e.g., air temperatures, humidity, and wind speeds) that drive net surface and bottom heat fluxes (J ) are limited over the scale of an individual reef (McGowan et al. 2010, Weller et al. 2008). Second, the capacities of different reef communities to absorb shortwave radiation (dependent on their albedo) generally vary by less than a factor of 2 (Hochberg et al. 2003). Third, a substantial fraction of shortwave radiation is absorbed by the water column itself, and this proportion increases with water depth. The end result is that spatial variation in bottom albedo resulting from a changing benthic reef habitat usually has only a secondary effect on the net heating or cooling of reef waters, even for very shallow reef systems (Zhang et al. 2013).

4. REGIONAL TO GLOBAL SCALES (>10 km) 4.1. Global Distribution of Wave and Tidal Forcing With only a few exceptions, studies have found that the circulation of reefs is dominantly forced by waves, or in some cases by tides (Andréfouët et al. 2006, Falter et al. 2013, Monismith 2007). Although the three-dimensional circulation of reef slopes and lagoons can be strongly influenced by local wind forcing (Atkinson et al. 1981, Wolanski & Thomson 1984) as well as by buoyancy forcing www.annualreviews.org • Oceanic Forcing of Coral Reefs


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Figure 4 Global spatial distributions and frequency distributions of (a,b) annual mean significant wave height (Hs ), (c,d ) mean tidal range (MTR), and (e,f ) relative tidal range (MTR/Hs ) for warm-water coral reef systems. Global coral reef distributions are from the 1-km-resolution data set from UNEP-WCMC (2003) and were joined with global wave height and tide distributions. Annual significant wave heights were derived using data from Young et al. (2011). Mean tidal ranges were computed from tidal harmonics derived from the Oregon State University Tidal Inversion Software (OTIS) (Egbert & Erofeeva 2002).

Macrotidal reef system: a reef system where the tidal range exceeds 3 m

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from thermal gradients (Monismith et al. 2006) or freshwater discharge (Hoeke et al. 2013), these effects tend to be dominant only on reefs protected from ocean swell or within the relatively deep lagoons of barrier reefs and atolls. There are strong regional differences in the global distribution of significant wave heights Hs within the ± 30◦ latitude band where warm-water coral reefs are found (Figure 4). Reefs in the Pacific and Indian Oceans tend to be dominantly wave forced (annual mean Hs > 1.5 m), whereas reefs in the Caribbean, Southeast Asia, and northern parts of Australia tend to experience only weak to moderate wave forcing (typical annual mean Hs < 1 m). These patterns likely drive substantial regional-scale differences in the wave-driven flows and residence times within reefs, depending, of course, on the morphologies of individual reefs within each region (see Section 3). Despite the dominance of wave-driven reef systems globally, there are still numerous reef systems worldwide that can be considered tide dominated, defined here simply as locations where the ratio of the mean tidal range (MTR) to the annual mean Hs is greater than 1 (Figure 4). Such systems have for the most part remained neglected in the literature; they include some extreme examples of macrotidal reef systems (MTR > 3 m) in regions off northern Australia, off east Africa, and off Central and South America (Figure 4). For example, in the Kimberley region of northwestern Australia, where numerous reefs are subject to tidal ranges greater than 10 m, water frequently drains off reef terraces as “waterfalls” during ebb phases of the tide (Figure 5). The dynamics of these tide-dominated reef systems, where the strongly varying flows lead to a critical flow point at the reef terrace that restricts flow, are fundamentally different from those of traditional wave-driven coral reef flows, in which flow resistance is due solely to bottom drag. A Lowe

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Figure 5 (a) A macrotidal reef system in the Kimberley region of northwestern Australia, where the spring tidal range reaches up to 10 m (photograph by R.J. Lowe). The photograph shows the reef at low tide with water draining off the coralline algal reef platform as a “waterfall.” (b) A schematic of water draining off an emergent macrotidal reef island at low tide.

much-improved understanding of tide-dominated reef systems is necessary to ultimately develop appropriate predictive models of these very distinct coastal flows. Whereas tidal forcing is predictable and quasi-stationary over long timescales (i.e., governed by set tidal harmonics), wave forcing on reefs is often episodic and subject to extreme events. Extreme wave events generated by tropical cyclones may be rare and short lived; however, the large wave heights and storm surges generated can have a profound and long-lasting impact on coral reef ecosystems. In addition, large extratropical cyclones in the major ocean basins may also transmit large swell waves across the ocean to remote reef systems thousands of kilometers away—as occurs, for example, when large waves generated by remote storms impart substantial wave energy to Pacific island reefs (Hench et al. 2008). Overall, it appears that, for many reefs,

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these extreme wave events play a primary role in shaping the reef community composition and zonation by establishing the mechanical limits of various reef organisms (Dollar & Tribble 1993, Grigg 1998, Lugo-Fernández & Gravois 2010, Madin & Connolly 2006). Other investigators have also argued that long-term trends in the frequency of extreme wave events can drive associated declines in coral coverage of reefs. For example, De’ath et al. (2012) argued that one major cause for the decline in coral coverage across the Great Barrier Reef over the past ∼30 years was the number of unusually strong tropical cyclones.


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4.2. Offshore Ocean Interactions with Reefs Offshore ocean dynamics are gaining increasing recognition for the critical role they play in driving many reef ecosystem processes (Freeman et al. 2012, Gove et al. 2013, Wyatt et al. 2012). Nevertheless, our quantitative understanding of how reefs are connected to the surrounding ocean remains poor owing to both the complex nature of these interactions and the lack of comprehensive studies that simultaneously consider reef ecosystem dynamics over a broad range of relevant scales (from regional down to community scales). At the broadest scale—that of entire ocean basins—the presence of major ocean boundary currents has long been known to regulate the distribution of many tropical coral reef systems globally. The general lack of major coral reef systems on the continental shelves of eastern ocean basins has been attributed largely to persistent upwellingfavorable conditions generated by wind-driven, equatorward-flowing eastern boundary currents that can inhibit the formation of oligotrophic tropical reefs (Birkeland 1997). In fact, many reefs across the globe depend on regional ocean currents to provide thermal conditions favorable for reef growth. Some good examples are the high-latitude coral reefs found between 28◦ S and 32◦ S off the coasts of eastern and western Australia (Lord Howe Island and the Houtman-Abrolhos Islands, respectively); these reef systems exist much farther south than those in other parts of the Southern Hemisphere owing to the poleward transport of heat by the East Australian Current and the Leeuwin Current. Nevertheless, predictions of how coral reef systems respond to global climate variability have tended to neglect how subtle changes in regional ocean circulation patterns may locally affect reefs in the future, instead tending to assume that reefs will be exposed only to ocean-basin-scale changes in temperature and carbonate chemistry (e.g., Hoegh-Guldberg et al. 2007, Silverman et al. 2009). A growing body of literature has described how a wide range of transient hydrodynamic processes on the shelf or slopes offshore of reefs influence shallow inshore reef systems. Multiple studies have identified coastal upwelling in particular as an important mechanism driving the cross-shelf exchange of nutrients between the ocean and many reefs; these studies include several that have examined how wind- or current-driven upwelling contributes substantial fluxes of subsurface nutrients to the Great Barrier Reef (Andrews & Gentien 1982, Brinkman et al. 2002, Wolanski et al. 1988) and to Ningaloo Reef off western Australia (Wyatt et al. 2010, 2012) as well as through the secondary flows generated by island wakes in the Pacific (Gove et al. 2006). Studies have also demonstrated that coastal upwelling significantly cools the coastal waters surrounding some coral reefs, suggesting that these regions could provide some refuge from increased ocean warming (e.g., Chollett & Mumby 2013, Karnauskas & Cohen 2012, Riegl & Piller 2003, Van Hooidonk et al. 2013). Indeed, frequent, episodic upwelling can locally reduce water temperatures by up to several degrees in reef systems ranging from northwestern Australia (Lowe et al. 2012) to the Caribbean, the Red Sea, and the eastern coastlines of Africa (Riegl & Piller 2003). Higher-frequency internal waves are similarly well known to drive substantial cross-shelf fluxes of nutrients, plankton, and heat both to and from many coral reefs. The most comprehensive observations of these dynamics have come from studies of internal waves off the Florida Keys (Davis 18.16

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et al. 2008; Leichter et al. 1996, 2003) and in French Polynesia (Leichter et al. 2012, Wolanski & Delesalle 1995). Despite the clear importance of internal waves to cross-shelf exchange in these regions, their specific influence on the nutrient and heat budgets of reefs in other parts of the world remains poorly known. Ultimately, our understanding of how shallow reef systems respond to the larger-scale dynamics of the surrounding ocean (including those driven by coastal upwelling, internal waves, coastal eddy fields, and episodic extreme events such as tropical cyclone mixing) remains primitive.

SUMMARY POINTS 1. The oceans influence the structure and function of coral reefs through a variety of mechanisms, ranging from small-scale boundary-layer dynamics occurring on submillimeter scales to regional circulation patterns spanning hundreds of kilometers. 2. Mass and momentum exchange within and above coral reef canopies can differ substantially depending on the prevailing flow regime. Under unconfined, unidirectional flow, flow within the canopy is driven primarily by a shear layer at the top of the canopy and is relatively weak. Under severely depth-limited flow or wave-driven oscillatory flow, flow within the canopy is driven primarily by pressure gradients and is much stronger. 3. Rates of dissolved nutrient and particle uptake by reef communities are heavily influenced by the predominant boundary-layer physics; however, mechanisms of particle trapping and feeding are highly varied, and their physics are still not well understood. 4. Circulation across most shallow reef systems is wave driven, with the tides acting as a secondary variable modulating wave-driven flows. However, in some regions the direct forcing of reef circulation by tides is much stronger than that by waves. 5. Spatial and temporal changes in reef water temperature and chemistry are intrinsically linked through a balance between the net fluxes of heat or mass that drive their nonconservative behavior and the circulation of reef waters. The circulation, residence times, and ages of reef waters are, in turn, spatially dependent on the hydrodynamic forces driving the flow as well as the particular morphology of a given reef system. 6. Episodic upwelling and internal waves can provide short-term (days) and intermediatescale (kilometers) mechanisms through which coral reefs are exposed to cooler and more nutrient- and/or plankton-rich waters. Longer-term changes in regional circulation patterns (weeks to months) can either provide conditions favorable for reef growth or help foment large-scale thermal stress events (tens to hundreds of kilometers).

FUTURE ISSUES 1. Predicting flow and drag forces within the complex and varied morphologies of reef canopies remains a major challenge. New experimental data sets and modeling approaches are needed to further advance predictions of reef canopy flows under both unidirectional and wave-driven conditions.

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2. Likewise, existing nearshore models neglect how bottom drag under waves and currents are influenced by in-canopy momentum dynamics. Improving the parameterizations of these canopy-scale dynamics, including coupling them within wave and circulation models, would no doubt substantially improve hydrodynamic models in reef applications.


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3. Although existing mass-transfer formulations provide some ability to predict rates of dissolved nutrient uptake by reef communities, there are still major gaps in our knowledge of nutrient mass transfer under wave-driven oscillatory flow. 4. Some empirical data on particle uptake rates by reef communities are available, but mechanistic approaches for modeling these dynamics are virtually nonexistent. The dependency of uptake rates on the mechanism of particle capture, as well as on the size and composition of the particles themselves, makes this a particularly challenging research endeavor. 5. Little is known about circulation around reefs with relatively large tidal ranges (mean tidal range of >3 m) and how this affects the spatial and temporal variation in reef metabolism and water quality. Such systems should be given greater attention. 6. Multiple studies over the past two decades have documented the short-term (days) impact of coastal upwelling and internal waves on the temperature, chemistry, and plankton communities of reef waters. However, our understanding of how important these episodic events are to the growth and structure of reef communities over the long term (months to years) is very limited, as is our understanding of how they are mechanistically linked to climate-driven changes in regional ocean dynamics.

DISCLOSURE STATEMENT The authors are not aware of any affiliations, memberships, funding, or financial holdings that might be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS We dedicate this review to Marlin Atkinson (1951–2013), who will be remembered as a pioneer in the study of ocean forcing of reef ecosystems and who helped inspire our own interest in this subject more than a decade ago. Through the years, we have learned much about coral reefs through collaboration with colleagues and friends in the research community, especially Stephen Monismith, Jeff Koseff, Eric Hochberg, Graham Symonds, Greg Ivey, Steve Smith, Frank Sansone, Mark Merrifield, Carlos Coimbra, Pascale Cuet, Alex Wyatt, Zhenlin Zhang, Malcolm McCulloch, Richard Brinkman, Chari Pattiaratchi, Dan Schar, Jerome Aucan, Christine Pequignet, Uri Shavit, Geno Pawlak, Serge Andréfouët, Frazer McGregor, Andrew Pomeroy, Mark Buckley, Ap van Dongeren, Dano Roelvink, Stuart Humphries, Ben Radford, Nicole Jones, Curt Storlazzi, Renee Gruber, Mike Cuttler, Gundula Winter, Edwin Drost, Soheila Taebi, Jim Hench, Johanna Rosman, Sam Kahng, Matt Reidenbach, and Sandy Chang. We also thank Stefan Zieger and Ian Young for providing the mean global wave height data used in Figure 3. Support for this work was provided by the Australian Research Council (ARC) Centre of Excellence for Coral Reef Studies (CE140100020). R.J.L. is also grateful for support from ARC under both the Future Fellowship (FT110100201) and Discovery Projects (DP140102026) schemes. This work 18.18

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was also partially supported by a grant from the Western Australia Marine Science Institution (WAMSI) under the Kimberley Marine Research Program. LITERATURE CITED Andersson AJ, Gledhill D. 2013. Ocean acidification and coral reefs: effects on breakdown, dissolution, and net ecosystem calcification. Annu. Rev. Mar. Sci. 5:321–48 Andréfouët S, Ouillon S, Brinkman R, Falter JL, Douillet P, et al. 2006. Review of solutions for 3D hydrodynamic modeling applied to aquaculture in South Pacific atoll lagoons. Mar. Pollut. Bull. 52:1138–55 Andréfouët S, Pagès J, Tartinville B. 2001. Water renewal time for classification of atoll lagoons in the Tuamotu Archipelago (French Polynesia). Coral Reefs 20:399–408 Andrews JC, Gentien P. 1982. Upwelling as a source of nutrients for the Great Barrier Reef ecosystems: a solution to Darwin’s question? Mar. Ecol. Prog. Ser. 8:257–69 Atkinson MJ, Bilger RW. 1992. Effect of water velocity on phosphate uptake in coral reef-flat communities. Limnol. Oceanogr. 37:273–79 Atkinson MJ, Falter JL. 2003. Coral reefs. In Biogeochemistry of Marine Systems, ed. KP Black, GB Shimmield, pp. 40–64. Boca Raton, FL: CRC Atkinson MJ, Smith S, Stroup E. 1981. Circulation in Enewetak atoll lagoon. Limnol. Oceanogr. 26:1074–83 Ayukai T. 1995. Retention of phytoplankton and planktonic microbes on coral reefs within the Great Barrier Reef, Australia. Coral Reefs 14:141–47 Baird ME, Atkinson MJ. 1997. Measurement and prediction of mass transfer to experimental coral reef communities. Limnol. Oceanogr. 42:1685–93 Barnes D, Devereux M. 1984. Productivity and calcification on a coral reef: a survey using pH and oxygen electrode techniques. J. Exp. Mar. Biol. Ecol. 79:213–31 Becker J, Merrifield M, Ford M. 2014. Water level effects on breaking wave setup for Pacific Island fringing reefs. J. Geophys. Res. 119:914–32 Bilger RW, Atkinson MJ. 1992. Anomalous mass transfer of phosphate on coral reef flats. Limnol. Oceanogr. 37:261–72 Birkeland C, ed. 1997. Life and Death of Coral Reefs. New York: Springer Brinkman R, Wolanski E, Deleersnijder E, McAllister F, Skirving W. 2002. Oceanic inflow from the Coral Sea into the Great Barrier Reef. Estuar. Coast. Shelf Sci. 54:655–68 Bruno JF, Siddon CE, Witman JD, Colin PL, Toscano MA. 2001. El Nino ˜ related coral bleaching in Palau, Western Caroline Islands. Coral Reefs 20:127–36 Buckley M, Lowe RJ, Hansen J. 2014. Evaluation of nearshore wave models in steep reef environments. Ocean Dyn. 64:847–62 Callaghan DP, Nielsen P, Cartwright N, Gourlay MR, Baldock TE. 2006. Atoll lagoon flushing forced by waves. Coast. Eng. 53:691–704 Chang S, Elkins C, Alley M, Eaton J, Monismith SG. 2009. Flow inside a coral colony measured using magnetic resonance velocimetry. Limnol. Oceanogr. 54:1819 Charpy L, Blanchot J. 1999. Picophytoplankton biomass, community structure and productivity in the Great Astrolabe Lagoon, Fiji. Coral Reefs 18:255–62 Chindapol N, Kaandorp JA, Cronemberger C, Mass T, Genin A. 2013. Modelling growth and form of the scleractinian coral Pocillopora verrucosa and the influence of hydrodynamics. PLoS Comput. Biol. 9:e1002849 Chollett I, Mumby PJ. 2013. Reefs of last resort: locating and assessing thermal refugia in the wider Caribbean. Biol. Conserv. 167:179–86 Cyronak T, Santos I, McMahon A, Eyre B. 2013. Carbon cycling hysteresis in permeable carbonate sands over a diel cycle: Implications for ocean acidification. Limnol. Oceanogr. 58:131–43 Darwin C. 1842. The Structure and Distribution of Coral Reefs. London: Smith Elder & Co. Davis KA, Leichter JJ, Hench JL, Monismith SG. 2008. Effects of western boundary current dynamics on the internal wave field of the Southeast Florida shelf. J. Geophys. Res. 113:C09010 Davis KA, Lentz SJ, Pineda J, Farrar JT, Starczak VR, Churchill JH. 2011. Observations of the thermal environment on Red Sea platform reefs: a heat budget analysis. Coral Reefs 30:25–36 www.annualreviews.org • Oceanic Forcing of Coral Reefs


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Genetic diversity and divergence among coastal and offshore reefs in a hard coral depend on geographic discontinuity and oceanic currents.

Fishing down nutrients on coral reefs.

Warm-water coral reefs and climate change.

Are coral reefs victims of their own past success?

Coral reefs on the edge? Carbon chemistry on inshore reefs of the great barrier reef.

Complex environmental forcing across the biogeographical range of coral populations.

Tradeoffs between fisheries harvest and the resilience of coral reefs.

Coral reefs. Limited scope for latitudinal extension of reef corals.

Inner Workings: Coral reefs at a tipping point.

Optimising Land-Sea Management for Inshore Coral Reefs.

Ophiuroidea (Echinodermata) from coral reefs in the Mexican Pacific.

Phase shift facilitation following cyclone disturbance on coral reefs.

Conservation Planning for Coral Reefs Accounting for Climate Warming Disturbances.

Positive Feedbacks Enhance Macroalgal Resilience on Degraded Coral Reefs.

Octocoral Species Assembly and Coexistence in Caribbean Coral Reefs.

Tropical dead zones and mass mortalities on coral reefs.

Keeping It Local: Dispersal Limitations of Coral Larvae to the High Latitude Coral Reefs of the Houtman Abrolhos Islands.

Presence of cleaner wrasse increases the recruitment of damselfishes to coral reefs.

Ecohydrodynamics of cold-water coral reefs: a case study of the Mingulay Reef Complex (western Scotland).

Redefining thermal regimes to design reserves for coral reefs in the face of climate change.

Diet and condition of mesopredators on coral reefs in relation to shark abundance.

Ghost reefs: Nautical charts document large spatial scale of coral reef loss over 240 years.

Impact of conservation areas on trophic interactions between apex predators and herbivores on coral reefs.

A new species of Nebalia (Crustacea, Leptostraca) from coral reefs at Pulau Payar, Malaysia.